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¹ Institute for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, MMU Cheshire, UK

	Abstract

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This study investigated changes in elderly muscle joint angle–torque relation induced by resistance training. Older adults were assigned to either training (n = 9, age 74.3 ± 3.5 years; mean ± S.D.) or to control groups (n = 9, age 67.1 ± 2 years). Leg-extension and leg-press exercises were performed three times per week for 14 weeks. Maximal isometric knee extension torque was measured across the knee joint angle range of movement. Vastus lateralis muscle architecture was examined in vivo using ultrasonography. The vastus lateralis muscle fascicle force was estimated from the measured joint torque, enabling construction of the fascicle length–force relation. Electromyographic (EMG) activity was measured from representative agonist and antagonist muscles. Training altered the angle–torque relation: (a) displacing it by 9–31% towards higher torque values (P < 0.05); and (b) shifting the optimal angle from 70 deg (corresponding torque: 121.4 ± 61 N m) before to 60 deg (134.2 ± 57.2 N m; P < 0.05) after training. Training also altered the fascicle length–force relation: (a) displacing it by 11–35% towards higher force values; and (b) shifting the optimal fascicle length from 83.7 ± 8 mm (corresponding force: 847.9 ± 365.3 N) before to 93.2 ± 12.5 mm (939.3 ± 347.8 N; P < 0.01) after training. The upward displacement of the angle–torque relation was mainly due to a training-induced increase in agonist activation, whilst the shift in the optimal angle was associated with changes in muscle-tendon properties.

(Received 7 April 2004; accepted after revision 13 August 2004; first published online 24 August 2004)
Corresponding author N. D. Reeves: Institute for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, MMU Cheshire, Hassall Road, Alsager, Cheshire, ST7 2HL, UK. Email: n.reeves{at}mmu.ac.uk

	Introduction

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Maximal muscle strength declines with age (Narici et al. 1991; Winegard et al. 1996), thereby reducing the strength reserve available to perform tasks of daily living and bringing elderly individuals closer to their ‘threshold for independence’ (Young & Skelton, 1994; Rantanen & Avela, 1997; Kozakai et al. 2000). Strength training in old age is an effective countermeasure against ageing-induced reductions in muscle strength (Frontera et al. 1988; Hakkinen et al. 1998a,b; Harridge et al. 1999; Tracy et al. 1999; Scaglioni et al. 2002). When training-induced adaptations in maximal muscle strength have been assessed in previous studies this has been done typically by measuring maximal isometric torque at a given joint angle (Frontera et al. 1988; Hakkinen et al. 1998a,b; Harridge et al. 1999; Scaglioni et al. 2002). The implicit assumption made in such studies that employ loading throughout the physiological range of movement is that training would not shift the angle–torque relation medio-laterally. If, however, this assumption is not correct and the optimal angle does in fact shift due to training, then erroneous conclusions might be reached regarding the effectiveness of training due to interangle differences in joint torque improvement.

In theory, the optimal angle and thus the entire angle–torque relation might change following strength training in old age. Torque is derived from the action of muscle forces on the skeleton, through anatomical levers (Lieber and Boakes, 1988). Maximal isometric torque is known to change as a function of joint angle (e.g. Sale et al. 1982; Kulig et al. 1984), and this relation depends upon: (a) the tendon moment arm length–angle relation; (b) the length–force relation of agonist muscles; and (c) the activation level of agonist and antagonistic muscles. The tendon moment arm length is a dimension determined by the anatomical constraints of the skeleton and therefore would not be altered by training. However, the muscle length–force relation might change after training because of two main reasons. First, although fascicle length is reduced with ageing (Narici et al. 2003), training may partly reverse this effect (Narici et al. 2000), presumably due to the addition of sarcomeres in series (Williams et al. 1988; Goldspink, 1998). Assuming that all other factors remain constant, this training-induced adaptation would cause a greater shortening of each sarcomere for the same whole muscle length shortening (Gans & Bock, 1965), as illustrated schematically in Fig. 1. Second, tendon stiffness is reduced with ageing (Maganaris, 2001b); but strength training has been shown to increase the stiffness of elderly human tendons (Reeves et al. 2003). Increased tendon stiffness would reduce fascicle shortening, thus shifting the average maximal sarcomere operating range to longer lengths. In vivo, an interaction would occur between the contrasting effects resulting from changes in fascicle length and tendon stiffness, complicating interpretation of the resultant effects on the length–force and angle–torque relations. Ageing reduces agonist activation (Yue et al. 1999) and increases antagonistic coactivation (Macaluso et al. 2002), but strength training partly reverses these effects (Hakkinen et al. 1998a, 2001; Harridge et al. 1999; Scaglioni et al. 2002). It remains unknown, however, if these training-induced changes in agonist–antagonist activation are joint angle-specific, which might therefore shift the optimal angle and thus alter the angle–torque relation.

View larger version (20K): [in this window] [in a new window]   Figure 1.  Schematic diagram showing the theoretical effect of differences in the number of sarcomeres in series on sarcomere shortening during an isometric contraction where muscle length shortening remains constant A greater number of sarcomeres in series (B) results in a greater shortening of each sarcomere as compared to the situation with fewer sarcomers in series (A).

	Methods

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Subjects

Eighteen volunteers (10 females and 8 males) gave written informed consent to participate in this study. All procedures used in this study complied with the declaration of Helsinki and were approved by the Ethics Committee from the Institute for Biophysical and Clinical Research into Human Movement at the Manchester Metropolitan University. Subjects received medical clearance from their general practitioners prior to initiating the training programme. Exclusion criteria for participation in the study were the presence of known neurological, musculoskeletal, inflammatory or metabolic disorders, uncontrolled hypertension or angina, or neoplastic disease. None of the subjects had previously taken part in any type of resistance training, but all were physically active, participating in activities such as bowling, gardening and walking. Five females and four males (n = 9, age 74.3 ± 3.5 years, body mass 69.7 ± 14.8 kg and height 1.63 ± 0.09 m, means ± S.D.) were assigned randomly to the training group, with the remaining five females and four males assigned to the non-training control group (n = 9, age 67.1 ± 2 years, body mass 73.5 ± 14.9 kg and height 1.68 ± 0.12 m).

Resistance training programme

Training was performed three times per week for 14 weeks using resistance exercise machines (Technogym, Gambettola, Forli, Italy). A general warm-up was performed on a cycle ergometer at 60–65% of the age-predicted maximum heart rate. Specific exercises performed were: (a) the bilateral leg-extension for the knee extensor muscle group; and (b) the bilateral leg-press for the hip, knee and ankle extensors. Other exercises were performed to provide an overall conditioning stimulus; these were the bilateral calf-raise, chest-press, seated-row, abdominal-crunch and lower back-extension. Subjects became familiarized with the exercises during the first 2 weeks of training, during which the workload was gradually increased until they were able to lift and lower, under control, the highest possible load five consecutive times (5-repetition maximum, 5 RM) for each exercise. It was considered that the 5 RM was more appropriate for elderly individuals who were unaccustomed to this type of strenuous exercise, as an alternative to the 1 RM. A similar approach of testing strength on the training devices using the 3–5 RM has been used previously for elderly individuals (Welle et al. 1995; Tracy et al. 1999; Scaglioni et al. 2002). The 5 RM was determined every 2 weeks to assess any strength increases. All exercises were performed with the concentric movement phase lasting 2 s followed by a 3 s eccentric movement phase. One specific warm-up set of 15 repetitions was performed for each exercise at an intensity of 45% of the 5 RM, followed by two or three sets of static stretching for specific muscle groups. For each of the lower limb exercises, two training sets of 10 repetitions were performed, initially at an intensity of 60–70% of the 5 RM, progressing to 80% of the 5 RM within 1–3 weeks dependent upon the subject's capabilities. According to the formula proposed by Brzycki (1993) for young adults, this intensity (80% of the 5 RM) corresponds to approximately 70–75% of the predicted 1 RM. A recovery period of 3 min was introduced between sets. Subjects were monitored very closely during training to ensure performance of the correct technique, whilst verbal encouragement was given to maintain motivation. Compliance to training was very high; only 7% of the sessions were missed.

Measurement of maximal isometric torque and voluntary activation capacity

Maximal isometric knee extension and flexion torque were assessed using an isokinetic dynamometer (Cybex NORM, New York, NY, USA) at nine knee joint angles ranging from 90 to 10 deg tested in a randomised order, in 10 deg increments (full extension = 0 deg), with the hip angle at 85 deg (supine position = 0 deg). With the right leg, one contraction was performed at each knee joint angle with 3 min rest between contractions. The centre of rotation of the knee joint was visually aligned with the dynamometer axis of rotation and straps were positioned at the hip, shoulders and over the right thigh to prevent any extraneous movement. Subjects had previously visited the laboratory on at least one occasion to become familiarized with the procedures involved. Subjects were instructed to perform a maximal isometric knee extension contraction in the absence of any visual feedback, by increasing their effort in a linear ramp fashion, so that maximal torque was reached after 2 s and then maintained until a verbal signal was given to stop. When the voluntary torque peaked, a superimposed supramaximal double twitch with 50 µs pulse width and 50 ms interstimulus gap was applied to the quadriceps muscle group through two 7.5 x 12.5 cm self-adhesive electrodes (Versa-Stim, CONMED, New York, NY, USA) placed on the distal and proximal regions of the thigh, using a constant current stimulator (Digitimer stimulator, model DS7, Welwyn Garden City, UK). To identify the stimulation intensity corresponding to maximal twitch torque, single twitches were applied at rest with increasing current intensity. The point at which a further increase in current by 50 mA failed to increase the twitch torque was defined as the supramaximal stimulation intensity. The voluntary activation capacity of the quadriceps muscle group was calculated as maximum voluntary torque/(maximum voluntary torque + superimposed stimulation torque), a method that has been previously applied using tetanic stimulation (Kent-Braun et al. 2002). The maximal voluntary torque data were selected as those developed immediately before the application of the stimuli.

Measurement of electromyographic activity

Electromyographic (EMG) activity was assessed from the vastus lateralis (VL) muscle and the long head of the biceps femoris (BF) muscle. Two self-adhesive Ag–AgCl electrodes 10 mm in diameter (Neuroline, Medicotest, Rugmarken, Denmark), were placed in a bipolar configuration with a constant interelectrode distance of 20 mm at a site corresponding to the distal third of the muscle length (SENIAM, 1999). Reference electrodes were placed on the lateral tibial condyle. In an attempt to minimize cross-talk from adjacent muscles, electrodes were placed along the mid-sagittal plane of each muscle, guided by axial-plane ultrasound scanning. Shaving, skin abrasion and cleaning with an alcohol-based solution always preceded electrode placement in order to reduce skin impedance below 5000 . The location of all electrodes with respect to the muscle length and anatomical landmarks was recorded and also traced onto an acetate sheet to ensure identical placement on subsequent sessions. The raw EMG signal was preamplified and filtered using high- and low-pass filters set at 10 and 500 Hz, respectively. The root mean square (r.m.s.) EMG activity of the BF and VL muscles was measured over a 50 ms time phase corresponding to maximal isometric knee extension torque and normalized for a 1 s time phase by multiplying the measured phase by a factor of 20. This measurement time phase (50 ms) yields an acceptable signal-to-noise ratio (Seniam, 1999). To estimate the level of antagonistic coactivation during isometric knee extension, the BF muscle was examined as representative of the knee flexors (Kellis & Baltzopoulos, 1999; Aagaard et al. 2000; Macaluso et al. 2002). The r.m.s. EMG activity of this muscle was measured during maximal isometric knee flexion performed at the same knee joint angle, over a 50 ms time phase corresponding to maximal torque and normalized for a 1 s time phase. The antagonistic torque of the knee flexors during a maximal isometric knee extension contraction was calculated assuming a linear r.m.s. EMG–torque relation validated in a previous report (Reeves et al. 2004), from the r.m.s. EMG–torque relation of the BF muscle when acting as an agonist (Kellis & Baltzopoulos, 1997).

Signals of torque, stimuli application and EMG activity were displayed on the screen of a computer (G4, Apple Computer, Cupertino, CA, USA), interfaced with an acquisition system (Acknowledge, Biopac Systems Inc., Santa Barbara, CA, USA) used for analog-to-digital conversion at a sampling frequency of 2000 Hz.

Measurement of muscle architecture

Real-time B-mode ultrasonography (ATL-HDI 3000, Bothell, USA) with a 7.5 MHz linear-array probe was used to examine the VL muscle architecture in vivo in the resting state and during maximal isometric contraction, at all knee joint angles tested. Scans were acquired in the mid-sagittal plane, at the mid-length of the VL muscle in all sessions, based on traces drawn on acetates and records of anatomical landmarks. This procedure was deemed necessary because, in contrast to data suggesting that several muscles in younger individuals display architectural homogeneity along and across the muscle belly (Narici et al. 1996; Maganaris & Baltzopoulos, 1999; Maganaris, 2003), there is currently no information regarding the architectural homogeneity of the VL muscle in elderly humans. The probe was coated with a water-soluble transmission gel to provide acoustic contact and was held in place using an external fixation device, secured by the experimenter. This device also served to disperse any pressure that might be caused by the probe on the dermal surface, thereby minimizing compression of underlying structures. The probe was placed onto an echo-absorptive external marker fixed on the skin. The line cast on the ultrasound image by the external marker indicated whether any movement of the probe occurred with respect to the scanned structure. If movement of the probe did occur, this would result in scanning a different region of the muscle and this trial would be omitted. Ultrasound was synchronized with the acquisition system by using an externally generated noise spike visible on both systems. Ultrasound scanning was maintained at or above 25 Hz and was recorded onto SVHS videotape for subsequent analysis. Ultrasound images were then acquired using frame-capture software (Adobe Premier version 5.1, Adobe Systems Inc., USA). Resting scans were selected for analysis by ensuring the absence of any EMG activity. Ultrasound scans corresponding to the maximal isometric knee extension torque were identified at all tested knee joint angles. The VL muscle fascicular paths were identified as the interspaces between the echoes arising from the perimysial tissue surrounding each fascicle. The ultrasound probe was orientated along the sagittal plane of fascicular paths both at rest and during maximal contraction to allow the entire visible length of the fascicle to be tracked clearly. The VL muscle fascicles generally extended off the ultrasound scan window and it was therefore necessary to estimate part of the fascicular trajectory. Using digitizing software (NIH image version 1.61, National Institutes of Health, Bethesda, MD, USA) the visible portion of the fascicle was measured and the remaining part was estimated assuming linear continuation of the fascicle and aponeurosis in the proximal direction. This method is associated with an error of 4% and the interday reliability of fascicle length measurements have yielded an intraclass correlation coefficient of 0.99 (Reeves et al. 2004). Pennation angle was defined as the angle between the fascicular path and the deep aponeurosis of the VL muscle. When fascicles inserted curvilinearly into the aponeurosis, pennation angles were measured as the tangent at the insertion of the fascicle into the aponeurosis (Maganaris et al. 1998). When fascicle curvature was present, it occurred mainly at the insertion of the fascicles into the deep aponeurosis. The accuracy of muscle architecture measurements assessed using ultrasound has previously been validated against direct anatomical inspection on cadavers (Kawakami et al. 1993; Narici et al. 1996).

Estimation of fascicle length–force relation

The VL muscle was examined as representative of the entire quadriceps muscle group. The VL muscle fascicle length–force relation was estimated by following a series of steps, using previously reported methods (Maganaris, 2001a, 2003).

(a) The sum of the maximal knee extension joint torque (maximal voluntary torque + superimposed stimulation torque) and the estimated coactivation torque from the knee flexors was divided by the patellar tendon moment arm length for each tested knee joint angle:

(1)

where F_PT is the estimated patellar tendon force, TQ_KE the maximal isometric knee extension torque, TQ_Coac the estimated coactivation torque of the knee flexors and MA_PT the patellar tendon moment arm length.

(b) The patellar tendon moment arm lengths were quantified using a 0.2 Tesla magnetic resonance imaging (MRI) scanner (E-Scan, Esaote Biomedica, Genoa, Italy). Sagittal-plane scans were acquired using a T1-weighted spin-echo sequence with the following scanning parameters: time to echo (TE), 26 ms; time of repetition (TR), 850 ms; field of view (FOV), 180 x 180 mm; matrix, 256 x 192; 4 mm slice thickness and 0.4 mm interslice gap. The patellar tendon moment arm length was defined as the perpendicular distance from the mid-point of the patellar tendon to the tibio-femoral contact point (Baltzopoulos, 1995) and was measured using digitizing software previously described. Due to constraints in the size of the available coil, it was only possible to image the knee joint in full extension. The previously reported ratios of the patellar tendon moment arm length between 0 deg and the knee joint angles tested (Baltzopoulos, 1995) were used to estimate the moment arm length for each subject. Mean values of the patellar tendon moment arm lengths are displayed in Table 1.

(d) The VL muscle fascicle force was estimated by dividing VL muscle force by the cosine of the angle of pennation of fascicles, measured during maximal isometric contraction at the specific knee joint angle as:

(2)

where F_Fasc is the estimated VL muscle fascicle force, F_VL the estimated force produced by the VL muscle and cos the cosine of the angle of pennation of the VL muscle fascicles during maximal isometric contraction.

The fascicle length–force relation was normalized with respect to the maximal fascicle length and maximal isometric fascicle force in each of the respective pre- and postconditions.

Study design

All subjects were tested at baseline. Subjects in the experimental group were retested after 14 weeks of strength training. The control group received no training and were retested after 14 weeks of their usual activities.

Statistical analysis

The data were checked for normality of distribution using the Kolmogorov–Smirnov test. Student's unpaired t test was used to test for differences between the training and control groups at baseline for all of the reported variables. Student's paired t test was used to test for differences in the 5 RM following training. A 2 x 2 factorial analysis of variance (ANOVA) was used to test for differences between groups (training vs. control) and time (pre- vs. postcondition) for all reported variables. A 2 x 2 x 9 factorial ANOVA was used to test for differences between groups (training vs. control), time (pre- vs. postcondition) and knee joint angles (90–10 deg). The changes in optimal joint angle and fascicle length were tested in both groups with a 2 x 2 ANOVA by using the values of optimal angle and length, respectively, taken from each individual subject in both pre- and postconditions. Tests were followed up with a post hoc analysis using the Scheffé procedure where necessary. Data are reported as means ± S.D.; the level of significance was accepted at P < 0.05.

	Results

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No differences (P > 0.05) existed in baseline measurements between the training and control groups for the reported variables, with the exception of knee flexor coactivation at knee joint angles of 70, 50 and 40 deg (P < 0.05).

Weight-lifting capacity

The 5 RM for the leg-extension exercise increased by 14%, from 43.5 ± 12 kg before to 49.4 ± 14.1 kg after the 14 weeks of training (P < 0.01). The 5 RM for the leg-press exercise increased by 23%, from 178.3 ± 44.7 kg before to 219.1 ± 55.4 kg following training (P < 0.01). Due to logistical constraints, weight-lifting capacity was not assessed in the control group, which may limit the sustainability of the increases observed in the training group.

Angle–torque relation

Maximal isometric knee extension torque increased after training by 9–31% across the range of knee joint angles tested (P < 0.05; Fig. 2A). In the control group, maximal isometric torque declined by 8–13% at knee joint angles of 90, 70, 60, 50 and 40 deg (P < 0.05; Fig. 2B). Training caused a shift in the optimal knee joint angle for torque generation by 10 deg in the direction of full extension. At baseline in the training group, the maximal isometric torque occurred at the knee joint angle of 70 deg (121.4 ± 61 Nm); however, after training the optimal angle was displaced to 60 deg (134.2 ± 57.2 Nm; P < 0.05; Fig. 2A). This knee joint angle (60 deg) was the position at which the largest absolute increase in isometric torque (17.5 Nm) occurred after training. In contrast to the training group, the optimal angle in the control group shifted by 10 deg in the knee flexion direction due to reductions in isometric torque at specific joint angles. Further analysis revealed that the mean reductions in torque in the control group were predominantly influenced by a substantial decline (11–26%) in a subgroup (n = 4) of the control subjects. These subjects showed a similar decline in VL muscle r.m.s. EMG activity (6–23%), thus indicating that the reduction in torque resulted from lower voluntary efforts.

View larger version (12K): [in this window] [in a new window]   Figure 2.  Isometric knee extension torque-angle relation for the training group (A) and the control group (B) Dashed and continuous lines show the optimal angle for torque generation before and after training, respectively. Values are means and S.D., significantly (*P < 0.05 and **P < 0.01) different between pre- and postconditions.

The voluntary activation capacity of the knee extensors increased by 3–6% (P < 0.05) after training at all tested knee joint angles, with the exception of 90 (3% increase) and 50 deg (4% increase), at which significance was not reached (Fig. 3A). In contrast, although there was a tendency for activation capacity to decrease, no significant changes were observed in the control group as a whole (1–3% reduction; Fig. 3B).

View larger version (10K): [in this window] [in a new window]   Figure 3.  Voluntary activation capacity of the knee extensors as a function of knee joint angle for the training group (A) and the control group (B) Values are means and S.D., showing significantly (*P < 0.05) increased activation capacity post-training.

View larger version (13K): [in this window] [in a new window]   Figure 4.  The vastus lateralis muscle r.m.s. EMG activity, during maximal isometric knee extension as a function of knee joint angle for the training group (A) and the control group (B) Values are means and S.D., showing significantly (*P < 0.05 and **P < 0.01) increased VL muscle r.m.s. EMG activity post-training.

View larger version (12K): [in this window] [in a new window]   Figure 5.  The estimated knee flexor coactivation during maximal isometric knee extension as a function of knee joint angle for the training group (A) and the control group (B) Values are means and S.D.

Training increased resting fascicle length by 8–10% at all knee joint angles tested (P < 0.01; Fig. 6A). The longest fascicles were observed with the knee joint angle at 90 deg and the shortest fascicles with the knee joint angle at 10 deg (Fig. 6A and B). The VL muscle fascicles were significantly longer by 10–18% during maximal isometric contraction at all knee joint angles tested, following training (P < 0.01; Fig. 6A). Fascicle shortening in the transition from rest to maximal isometric contraction was reduced over the range of tested knee joint angles after training (Fig. 6A) and reached significance at the knee joint angles of 60 (pretraining, 10% shortening; post-training, 7% shortening), 50 (pretraining, 11% shortening; post-training, 6% shortening), 20 (pretraining, 16% shortening; post-training, 9% shortening) and 10 deg (pretraining, 16% shortening; post-training, 9% shortening). In contrast, no significant changes in resting fascicle length, fascicle length during maximal isometric contraction, or fascicle shortening in the transition from rest to maximal isometric contraction occurred in the control group (Fig. 6B).

View larger version (14K): [in this window] [in a new window]   Figure 6.  The VL muscle fascicle lengths at rest and during maximal isometric contraction as a function of knee joint angle for the training group (A) and the control group (B) Values are means, showing significantly (**P < 0.01) longer fascicles post-training. Filled bars represent the maximal S.D. values.

View larger version (14K): [in this window] [in a new window]   Figure 7.  The VL muscle pennation angles at rest and during maximal isometric contraction as a function of knee joint angle for the training group (A) and the control group (B) Values are means, with significantly (**P < 0.01) greater pennation angles post-training. Filled bars represent the maximal S.D. values.

View larger version (12K): [in this window] [in a new window]   Figure 8.  The estimated maximal isometric VL muscle fascicle force-length relation for the training group (A) and the control group (B) Dashed and continuous lines show the optimal length for fascicle force generation before and after training, respectively. Values are means and S.D., showing significant (*P < 0.05 and **P < 0.01) differences between pre- and postconditions.

View larger version (8K): [in this window] [in a new window]   Figure 9.  The estimated normalized (with respect to the maximal fascicle length and force in both pre- and postconditions) maximal isometric VL muscle fascicle length–force relation for the training group (A) and the control group (B) Values presented are means.

	Discussion

Top Abstract Introduction Methods Results Discussion References

The upward displacement of the angle–torque relation reflected an increase in torque occurring at every knee joint angle tested and is consistent with the increased weight-lifting capacity following training. Despite the lack of comparative data in the control group, the relative increase in weight-lifting capacity observed in the training group (14 and 23% for the leg-extension and leg-press exercises, respectively) is comparable to some previous reports on the effects of strength training programmes of similar duration in elderly individuals (Tracy et al. 1999; Scaglioni et al. 2002). Other studies, however, have shown much greater increases in weight-lifting capacity, ranging from 42 to 174% (Frontera et al. 1988; Welle et al. 1995; Harridge et al. 1999). These contrasting findings may be due to: (a) differences in the mean age and especially pretraining sedentary status of subjects between studies; and (b) the possibility that the initial 2 week familiarization period employed in the present study might have induced neural adaptations transferring to increased weight-lifting capacity (Hakkinen et al. 1998b).

The postintervention measurements showed that the angle–torque relation shifted by 10 deg in opposite directions in the training and control groups; in the full knee extension direction in the training group and in the knee flexion direction in the control group. As explained earlier, the latter finding may be accounted for by the exertion of submaximal voluntary efforts in some of the control subjects. The findings from the training group clearly show that the increase in torque was not constant across joint angles, which means that by assessing isometric torque at just a single joint position, as previous studies have done (Frontera et al. 1988; Hakkinen et al. 1998a,b; Harridge et al. 1999; Scaglioni et al. 2002), the maximum strength increase occurring following training would have been underestimated. This is particularly relevant when assessing the effectiveness of resistance training for increasing maximal strength in the elderly relative to their ‘threshold for independence’ (Young & Skelton, 1994; Rantanen & Avela, 1997; Kozakai et al. 2000). It might be suggested that the observed shift in the optimal angle could be the result of greater loading at specific joint angles in the range of motion during training. However, the training employed in the present study was performed using isotonic exercise devices. These machines are designed to maintain a constant external load throughout the range of movement. Hence, the explanation that differences in loading levels at certain positions in the range of movement might have contributed to the observed shift in the optimal angle is not tenable.

In an attempt to understand the origin of the changes in the angle–torque relation following training, investigation of the determinants are required; this is addressed in the following sections.

Activation of agonist and antagonist muscles

Voluntary activation capacity of the knee extensors was incomplete before training (90%), which is consistent with a previous report in the same muscle group (Harridge et al. 1999). However, activation capacity was lower in the previously mentioned study, ranging from 69 to 93%, most probably due to the much higher age (range 85–97 years) and sedentary status of subjects, which may preclude direct comparisons with the present study. In other muscle groups, however, studies have shown that older adults are capable of reaching high activation levels without any physical training (for example, 95% in the plantarflexors [Scaglioni et al. 2002], 99% in the dorsiflexors [Connelly et al. 1999; Kent-Braun & Ng, 1999; Kent-Braun et al. 2002] and 94–98% in the elbow flexors [Brown et al. 1990; Yue et al. 1999]), which suggests that the degree of activation may be muscle specific. Whilst voluntary activation capacity still remained incomplete after training in the present study, it did increase by an average of 4%, most probably through an increased number of recruited motor units and/or an increase in their firing frequency (Patten et al. 2001). This increase in activation capacity is similar in magnitude to a previous report in the plantarflexors following resistance training (Scaglioni et al. 2002). Although the observed increase ranged between 3 and 6% across the range of tested knee joint angles, no knee joint angle-specific changes were found (Fig. 3A).

In the present study we quantified activation capacity by following an approach independent of resting twitch measurements. An alternative approach frequently used to assess activation capacity is the twitch interpolation technique, which encompasses the resting twitch torque (Harridge et al. 1999; Scaglioni et al. 2002). An implicit assumption of this technique therefore is that in both conditions (at rest and during voluntary contraction) the stretch applied to the series elastic component (SEC) by the twitch is equivalent. This assumption, however, is clearly invalid because, in contrast to the resting state where there is no or little passive stretch, the SEC during a maximal effort contraction is considerably stretched by the shortening of the muscle. The effect of artificially changing SEC compliance on twitch torque has been experimentally confirmed (Loring & Hershenson, 1992), and similar results are to be expected with ‘physiologically induced’ changes in SEC compliance by changing joint position. As the knee joint angle moves from 90 deg towards full extension the muscle–tendon complex becomes progressively slacker, requiring a longer time period to stretch the SEC and develop torque. This effect would cause the resting twitch torque to decline progressively over the range of knee joint angles, thus influencing activation capacity when calculated using the twitch interpolation technique. To assess the degree of outcome difference between the two techniques, both techniques were applied in a subsample of subjects at a 90 deg knee joint angle. The results revealed that the voluntary activation capacity was 8% lower when calculated using the twitch interpolation technique as opposed to the method used in the present study. Whilst it is difficult to suggest that one particular method over- or under-estimates activation capacity, the results yielded by the approach followed in the present study are not adversely affected by the factors influencing the twitch interpolation technique. However, we recognize that the percutaneous stimulation protocol we employed may not have activated the entire knee extensor muscle mass. It has been suggested that by using percutaneous stimulation up to 60% of the muscle may be activated (Rutherford et al. 1986) but, considering the smaller muscle mass in elderly individuals, the percentage of the muscle activated in the present study may have in fact been higher than 60%. Superimposed tetanic stimulation would generate higher forces compared to a train of two stimuli, but it is associated with a greater level of discomfort.

Consistent with the increase in activation capacity, the VL muscle r.m.s. EMG activity increased after training (Fig. 4A). This observation is in line with previous findings (Hakkinen et al. 1998a, b), and suggests an increased neural drive. Again, there was no knee joint angle specificity observed in the training-induced changes in the VL muscle r.m.s. EMG activity. Taken together, the above results suggest that although the training-induced changes in neural drive might have contributed to the upward shift of the angle–torque relation, they would have no effect in displacing the optimal angle.

At any given knee joint angle, the level of knee flexor coactivation was unaltered after training (Fig. 5A), thus indicating that coactivation did not affect the changes in the angle–torque relation. This finding contrasts with previous reports in young and older adults (Carolan & Cafarelli, 1992; Hakkinen et al. 1998a, 2001). The coactivation levels observed are similar to those reported in elderly individuals (Hakkinen et al. 1998a), but are much higher than those reported in young adults (Carolan & Cafarelli, 1992), possibly indicating a greater need for the knee flexors to assist the anterior cruciate ligament in maintaining knee joint stability in the elderly (Draganich et al. 1989). The finding of a high coactivation level clearly stresses the need to account for the action of antagonistic muscles when estimating agonist muscle forces in elderly individuals; failure to do so would considerably underestimate agonist muscle forces. It should be noted that the presence of a substantial subcutaneous fat layer covering the muscle would increase the EMG cross-talk from neighbouring muscles (Solomonow et al. 1994). However, there was no significant difference in the fat layer measured using skinfold calipers at mid-thigh level post-training, indicating that any errors introduced by this situation would not affect the pre- to postintervention comparisons.

In contrast to the activation capacity data, the r.m.s. EMG activity of both agonists and antagonists changed as a function of knee joint angle. These findings are in agreement with previous reports in the knee extensors (Salzman et al. 1993) and might partly be accounted for by movement of the muscle innervation zone beneath the recording electrodes induced by joint rotation, as demonstrated by previous studies (Farina et al. 2001).

Fascicle length–force relation and muscle architecture

Figures 8 and 9 indicate that the fascicle length–force relation of the VL muscle in vivo extends over a part of the ascending limb, the entire plateau region and a part of the descending limb of the length–tension relation, consistent with previous reports from cadaver-based measurements (Cutts, 1988). Training altered the fascicle length–force relation, shifting the curve upwards and to the right (Fig. 8A). This indicates that after training: (a) a greater fascicle force was produced at the corresponding knee joint angle; and (b) it was possible to develop the same pretraining fascicle force at longer fascicle lengths. The former effect reflects a training-induced increase in neural drive. Increases in functional muscle size might have contributed to the upward displacement of the fascicle length–force relation; however, in the same group of subjects we have previously reported that the VL muscle physiological cross-sectional area (PCSA) remains unchanged after training because increases in muscle volume are accompanied by similar relative increases in fascicle lengths (Reeves et al. 2004). The latter effect corresponds to a training-induced shift of the optimal fascicle length for force generation by 10 mm in the opposite direction to that occurring in the angle–torque relation. The observation that the optimal knee joint angle for torque generation shifted to shorter muscle lengths following training might lead to inferences that the fascicle length–force relation shifted in a similar way. However, in vivo analysis of muscle structure performed in the present study demonstrates that this assumption is not tenable since the same knee joint angle corresponded to longer fascicle lengths after training. Due to changes in activation level pre- to post-training, if the fascicle length–force relation had been estimated based on voluntary torque data alone, this would not represent the maximal force-producing capability of the muscle. However, all data relating to the fascicle length–force relation were obtained at the time point of supramaximal stimulation (maximum voluntary torque + superimposed stimulation torque), therefore this approach partly circumvents the problem presented by variations in force due to incomplete voluntary activation.

The origin of the training-induced shift in the fascicle length–force relation may relate to changes in: (a) the length of muscle fascicles; and (b) the mechanical properties of the tendon.

(a) Resting fascicle length increased following training (Fig. 6A), suggesting the addition of sarcomeres in series. This is consistent with previous reports showing that mechanical overload is a powerful stimulant of protein synthesis, resulting in the addition of serial sarcomeres (Williams et al. 1988; Goldspink, 1998, 1999). Resting VL muscle fascicle lengths in the present study are shorter compared to those measured in young adults (Fukunaga et al. 1997), suggesting an ageing-induced loss of sarcomeres in series. In fact, analysis of in vivo scans from young and elderly muscles has previously shown that fascicle lengths are reduced in old age (Narici et al. 2003). However, the present results suggest that the ageing-induced reductions in fascicle length might be reversed by a period of strength training. This is consistent with a previous report of increased fascicle lengths following strength training in elderly individuals (Narici et al. 2000).

(b) We have previously shown in the same subject group that elderly tendons increase their tensile stiffness in response to resistance training (Reeves et al. 2003). Further support for the notion that tendon stiffening occurred due to training is given by the changes in muscle architecture during contraction. Since the tendon is in series with the muscle, the degree of fascicle shortening induced by contraction is dictated primarily by the elongation of the tendon. Following training, resting fascicles were longer, but fascicle shortening was in fact reduced, despite the development of even greater muscle forces. Consistent with reduced fascicle shortening, training reduced the pennation angle increase by contraction.

The shift in the fascicle length–force relation to longer lengths after training may be explained by the increased length of fascicles and the maintenance of their longer lengths upon contraction due to increases in tendon stiffness. Notwithstanding the training-induced shift of the absolute fascicle length–force curve, the pre- and post-training normalized curves were almost superimposed upon one another (Fig. 9A). This suggests that, despite increased fascicle lengths, the VL muscle remained operating over the same portion of the sarcomere length–tension relation (Fig. 10). However, for a given sarcomere length and shortening of absolute whole muscle length, if fascicle length increased (due to a greater number of sarcomeres in series) it would cause a greater shortening of each sarcomere (see Fig. 1), resulting in a left shift of the sarcomere length–tension relation (Gans & Bock, 1965). In contrast, increased tendon stiffness alone would reduce muscle fibre shortening, thus causing a right shift of the sarcomere length–tension relation (Gans & Bock, 1965; Zajac, 1989). It may be the case that these resultant right and left shifts cancel each other out, enabling the muscle to operate effectively over the same portion of the length–tension relation. Hence, despite the shift in the absolute fascicle length–force relation, it appears that when elderly skeletal muscle is subjected to increased loading, natural strategies might take place to ensure that it exerts maximal force over the same sarcomere length range (Fig. 10).

View larger version (14K): [in this window] [in a new window]   Figure 10.  Theoretical sarcomere length–tension relation based on the sliding filament theory of contraction (Huxley, 1957; Gordon et al. 1966) Sarcomere lengths are based on data taken from humans (Walker & Schrodt, 1974). The shaded lines above and below the ascending limb, plateau region and descending limb represent the theoretical maximal working range of the VL muscle, before and after training, respectively. Theoretical maximal working range was calculated by: (a) dividing the fascicle length at maximal force by an average (2.73 µm) optimal sarcomere length (Walker & Schrodt, 1974) to obtain the estimated number of sarcomeres in series present; and (b) estimating the sarcomere length at the extreme positions of force production from the estimated number of sarcomeres in series.

In conclusion, a regimen of increased loading in old age altered the knee extensor angle–torque relation causing: (a) a displacement to higher torque values; and (b) a shift in the optimal angle in the knee extension direction. Training also altered the fascicle length–force relation causing: (a) a displacement to higher force values; and (b) a shift in the optimal length for fascicle force generation to longer lengths. The increased torque produced after training was mainly due to increased agonist activation, whilst the shift in the optimal angle was associated with changes in muscle-tendon properties.

	References

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